Table 1.
A list of functionally verified soybean transcription factors involved in salt tolerance
| Gene | Phenotype | Functions | References |
|---|---|---|---|
| bHLH transcription factor | |||
| GmbHLH3 | Overexpression in Arabidopsis and soybean hairy roots enhances salt tolerance | GmbHLH3 regulates the expression of GmCLC1, which in turn retains NaCl in the root to prevent salt damage in the shoot | (Liu et al. 2022) |
| bZIP transcription factors | |||
| GmbZIP1 | Overexpression in Arabidopsis, wheat and tobacco enhances salt tolerance | GmbZIP1 regulates the expressions of ABA- and stress-related genes to mediate the ABA response | (Gao et al. 2011) |
| GmbZIP2 | Overexpression in Arabidopsis and soybean hairy roots enhances salt tolerance | Ectopic expression of GmbZIP2 can enhance the expressions of stress-responsive genes under normal conditions, salt stress, and mannitol treatment | (Yang et al. 2020b) |
| GmbZIP15 | Overexpression in Arabidopsis and soybean results in increased salt sensitivity | GmbZIP15 positively regulates the transcription of GmSAHH1 and negatively regulates GmWRKY12 and GmABF1 under abiotic stress | (Zhang et al. 2020a) |
| GmbZIP19 | Overexpression in Arabidopsis and soybean results in increased salt sensitivity | GmbZIP19 upregulates ABA-, JA-, ET-, and SA-inducible marker genes by interacting with their promoters but downregulates salt- and drought-responsive genes | (He et al. 2020a) |
| GmbZIP44, GmbZIP62, GmbZIP78 | Overexpression in Arabidopsis enhances salt tolerance | GmbZIP44, GmbZIP62, and GmbZIP78 mediate ABA signaling by upregulating ABI1 and ABI2 which regulate downstream stress-responsive genes | (Liao et al. 2008c) |
| GmbZIP110 | Overexpression in Arabidopsis and soybean hairy roots enhances salt tolerance | GmbZIP110 alters the expressions of stress-related genes in the ABA-signaling pathway and those related to ion transportation | (Xu et al. 2016) |
| GmbZIP132 | Overexpression in Arabidopsis enhances salt tolerance at germination stage | GmbZIP132 promotes the transcription of stress-responsive genes including RD29B, DREB2A, and P5CS | (Liao et al. 2008a) |
| GmbZIP152 | Overexpression in Arabidopsis enhances salt tolerance | GmbZIP152 activates antioxidant enzymes and the transcription of biotic and abiotic stress-related marker genes when stressed. GmbZIP152 can bind directly to the promoters of ABA-, JA-, ET-, and SA-inducible genes | (Chai et al. 2022) |
| GmFDL19 | Overexpression in soybean enhances salt tolerance | GmFDL19 reduces Na+ accumulation and enhances expression of ABA- and stress-responsive genes | (Li et al. 2017b) |
| GmTGA13 | Overexpression in Arabidopsis and soybean hairy roots enhances salt tolerance | GmTGA13 mediates ion homeostasis by facilitating K+ and Ca2+ absorption | (Ke et al. 2022) |
| GmTGA17 |
Overexpression in Arabidopsis and soybean hairy roots enhances salt tolerance RNAi soybean hairy roots show increased salt sensitivity |
GmTGA17 upregulates ABA-responsive genes and regulates ABA signaling under salt and drought stress | (Li et al. 2019a) |
| Dehydration-responsive element-binding (DREB) proteins | |||
| GmDREB1 | Overexpression in alfalfa enhances salt tolerance | Transgenic alfalfa exhibits a higher level of P5CS transcripts, which is consistent with a higher level of free proline | (Jin et al. 2010) |
| GmDREB2 | Overexpression in Arabidopsis enhances salt tolerance | GmDREB2 can induce the expressions of downstream genes RD29A and COR15a | (Chen et al. 2007) |
| GmDREB3 | Overexpression in Arabidopsis and tobacco enhances salt tolerance | GmDREB3 can bind to DREs and activate downstream genes | (Chen et al. 2009) |
| GmDREB6 | Overexpression in soybean enhances salt tolerance | GmDREB6 can enhance the expression of GmP5CS and increase the proline content when under salt stress | (Nguyen et al. 2019) |
| Ethylene-responsive factors (ERFs) | |||
| GmERF3 | Overexpression in tobacco enhances salt tolerance | GmERF3 can interact with the GCC box and DRE/CRT and activate the associated genes | (Zhang et al. 2009) |
| GmERF4 | Overexpression in tobacco enhances salt tolerance | GmERF4 possesses GCC-box- and DRE/CRT-binding specificities and inhibits the expressions of GCC-box-containing genes | (Zhang et al. 2010) |
| GmERF7 | Overexpression in tobacco enhances salt tolerance | GmERF7 functions as a transcription activator through binding to the GCC box of its target genes | (Zhai et al. 2013) |
| GmERF057, GmERF089 | Overexpression in tobacco enhances salt tolerance | GmERF057 and GmERF089 are induced by salt, drought, ET, SA, JA, and ABA, suggesting that they may be involved in various stress signaling pathways | (Zhang et al. 2008) |
| GmERF75 | Overexpression in Arabidopsis and soybean hairy roots enhances salt tolerance | GmERF75 is induced in SA, JA, and ET treatments, suggesting its role in integrating the signals from SA and ET/JA pathways | (Zhao et al. 2019b) |
| GmERF135 | Overexpression in Arabidopsis and soybean hairy roots enhances salt tolerance | GmERF135 regulates ET and ABA signaling by activating ET-producing genes, AtACO4, AtACS2, and ABA biosynthesis genes, ABA1, ABA2 | (Zhao et al. 2019c) |
| GRAS transcription factor | |||
| GmGRAS37 |
Overexpression in soybean hairy roots enhances salt tolerance RNAi soybean hairy roots show increased salt sensitivity |
GmGRAS37-overexpressing plants show upregulated GmDREB1, GmNCED3, GmCLC1, GmSOS1, and GmSODs under salt stress, so it can regulate ABA biosynthesis, ion transportation and ROS scavenging | (Wang et al. 2020) |
| Early Flowering 3 | |||
| GmJ |
Overexpression in soybean hairy roots enhances salt tolerance NIL-j soybean hairy roots show increased salt sensitivity |
J is involved in the regulation of downstream salt-responsive genes, including GmWRKY12, GmWRKY27, GmWRKY54, GmNAC11, and GmSIN1 | (Cheng et al. 2020) |
| MYB transcription factors | |||
| GmMYB12 | Overexpression in Arabidopsis enhances salt tolerance | GmMYB12 activates gene expressions and enzymatic activities of P5CS, SOD, and POD upon salt stress, and therefore helps maintain the proper levels of proline and ROS | (Wang et al. 2019b) |
| GmMYB12B2 | Overexpression in Arabidopsis enhances salt tolerance | GmMYB12B2 can increase the expressions of salt stress-responsive genes including DREB2A and RD17 | (Li et al. 2016b) |
| GsMYB15 | Overexpression in Arabidopsis enhances salt tolerance | GsMYB15 reduces the transcript levels of ABA marker genes (ABIs) and activates several TFs, conferring salt tolerance | (Shen et al. 2018a) |
| GmMYB46 | Overexpression in Arabidopsis enhances salt tolerance | GmMYB46 induces the expressions of salt-responsive genes, P5CS1, SOD, POD, and NCED3 to turn on salt tolerance mechanisms | (Liu et al. 2021b) |
| GmMYB68 |
Overexpression in soybean enhances salt tolerance RNAi soybean shows increased salt sensitivity |
GmMYB68 activates FBP and P5CR to promote the accumulation of soluble sugars and free proline | (He et al. 2020b) |
| GmMYB76, GmMYB92, GmMYB177 | Overexpression in Arabidopsis enhances salt tolerance | All three genes lead to the activation of DREB2A, RD17, and P5CS. In addition, GmMYB76 and GmMYB177 can enhance the expressions of RD29B, ERD10, and COR78 | (Liao et al. 2008b) |
| GmMYB81 | Overexpression in Arabidopsis enhances salt tolerance at germination stage | GmMYB81 regulates stress tolerance together with abiotic stress regulator GmSGF14l | (Bian et al. 2020) |
| GmMYB84 | Overexpression in Arabidopsis and soybean enhances salt tolerance | GmMYB84 can bind to the cis-regulatory sequence of GmAKT1 to mediate K+ transport and in turn establish a higher [K+]/[Na+] ratio | (Zhang et al. 2020b) |
| GmMYB118 |
Overexpression in Arabidopsis and soybean hairy roots enhances salt tolerance CRISPR-edited soybean shows increased salt sensitivity |
GmMYB118 regulates the expressions of stress-associated genes to reduce ROS and MDA levels under salt and drought stress | (Du et al. 2018) |
| GmMYB133 | Overexpression in Arabidopsis enhances salt tolerance | GmMYB133 confers salt tolerance through inducing the expression of salt tolerance-related genes including EARL1, MPK3 and AZI1 | (Shan et al. 2021) |
| GmMYB173 |
Overexpression in soybean roots enhances salt tolerance RNAi soybean roots show increased salt sensitivity |
Phosphorylated GmMYB173 has a higher affinity to the promoter of GmCHS5 and facilitates the accumulation of dihydroxy B-ring flavonoids | (Pi et al. 2018) |
| GmMYB183 |
Overexpression in soybean hairy roots shows increased salt sensitivity RNAi soybean hairy roots have enhanced salt tolerance |
GmMYB183 regulates GmCYP81E11 and enhances the accumulation of ononin, which has negative effects on soybean salt tolerance | (Pi et al. 2019) |
| NAC transcription factors | |||
| GmNAC06 |
Overexpression in Arabidopsis and soybean hairy roots enhances salt tolerance CRISPR-edited soybean hairy roots show increased salt sensitivity |
GmNAC06 promotes the expressions of GmUBC2 and GmHKT1 to maintain ion homeostasis and mediate oxidative stress responses | (Li et al. 2021b) |
| GmNAC15 | Overexpression in soybean hairy roots enhances salt tolerance | GmNAC15 regulates osmolyte biosynthesis to eliminate osmotic stress and induces the expressions of stress-responsive genes including GmERF3 and GmWRKY54 | (Li et al. 2018b) |
| GmNAC11 | Overexpression in Arabidopsis and soybean hairy roots enhances salt tolerance | GmNAC11 is involved in the regulation of DREB1A and other stress-associated genes | (Hao et al. 2011) |
| GmNAC20 | Overexpression in Arabidopsis enhances salt tolerance | GmNAC20 activates the DREB/CBF-COR pathway | (Hao et al. 2011) |
| GmNAC085 | Overexpression in soybean enhances salt tolerance | GmNAC085 enhances the expressions of stress-related genes involved in proline biosynthesis, Na+ transport, and dehydrin accumulation | (Hoang et al. 2021) |
| GmNAC109 | Overexpression in Arabidopsis enhances salt tolerance | GmNAC109 increases the transcript levels of stress-responsive genes such as DREBs, AREBs, RD29A, and COR15A. ABA-responsive genes, ABIs, and auxin-related genes, AIR3 and ARF2, are also induced | (Yang et al. 2019) |
| GmSIN1 |
Overexpression in soybean enhances salt tolerance RNAi soybeans show increased salt sensitivity |
GmSIN1 enhances the expressions of GmNCED3s and GmRbohBs, forming a positive feed-forward loop to amplify the initial salt stress signal by rapidly accumulating ABA and ROS | (Li et al. 2019b) |
| NF-YA transcription factors | |||
| GmNFYA |
Overexpression in soybean enhances salt tolerance RNAi soybean hairy roots show increased salt sensitivity |
Stress-induced GmNFYA destabilizes the GmFVE-GmHDA13 complex by interacting with GmFVE, resulting in the activation of salt stress-responsive genes by histone acetylation | (Lu et al. 2021) |
| GmNFYA13 |
Overexpression in Arabidopsis and soybean enhances salt tolerance RNAi soybeans show increased salt sensitivity |
GmNFYA13 can bind to and regulate the transcription of GmSALT3, GmMYB84, GmNCED3, and GmRbohB | (Ma et al. 2020) |
| Plant homeodomain finger protein | |||
| GmPHD2 | Overexpression in Arabidopsis enhances salt tolerance | GmPHD2 may downregulate several negative regulators of stress response-related genes such as CBF2, STRS1, and STRS2 | (Wei et al. 2009) |
| RAV transcription factor | |||
| GmRAV-03 | Overexpression in Arabidopsis enhances salt tolerance | (Zhao et al. 2017) | |
| Trihelix transcription factors | |||
| GmGT-2A, GmGT-2B | Overexpression in Arabidopsis enhances salt tolerance | The two GmGTs induce the stress tolerance genes, STZ/ZAT and DREB2A, and activate antioxidative mechanisms. Furthermore, GmGT-2B can enhance the expressions of ABA-dependent genes including NCED3, LTP3, LTP4 and PAD3 | (Xie et al. 2009) |
| VOZ transcription factor | |||
| GmVOZ1G |
Overexpression in soybean hairy roots enhances salt tolerance RNAi soybean hairy roots show increased salt sensitivity |
GmVOZ1G enhances the activities of POD and SOD under drought and salt stress | (Li et al. 2020a) |
| WRKY transcription factors | |||
| GmWRKY12 | Overexpression in soybean hairy roots enhances salt tolerance | The promoter of GmWRKY12 contains cis-acting elements including ABER4, MYB, MYC, GT-1, W-box, GARE, and DPBF, suggesting the role of GmWRKY12 in various stress and hormone responses | (Shi et al. 2018) |
| GmWRKY13 | Overexpression in Arabidopsis leads to increased salt sensitivity | GmWRKY13 upregulates ARF6 to promote lateral root development and ABI1 to mediate ABA response | (Zhou et al. 2008) |
| GmWRKY16 | Overexpression in Arabidopsis enhances salt tolerance | GmWRKY16 enhances the expressions of WRKY8, KIN1, and RD29A in salt stress | (Ma et al. 2019) |
| GmWRKY27 |
Overexpression in soybean hairy roots enhances salt tolerance RNAi soybean hairy roots show increased salt sensitivity |
GmWRKY27 interacts with GmMYB174 and inhibits the expression of GmNAC29, which negatively regulates stress tolerance | (Wang et al. 2015) |
| GmWRKY45 | Overexpression in Arabidopsis enhances salt tolerance | (Li et al. 2020b) | |
| GmWRKY49 | Overexpression in Arabidopsis and soybean enhances salt tolerance | GmWRKY49 can bind directly to the W-box and possibly modulates the expressions of downstream stress-related genes | (Xu et al. 2018) |
| GmWRKY54 | Overexpression in Arabidopsis enhances salt tolerance | GmWRKY54 regulates the expressions of DREB2A and STZ/Zat10 by binding to the W-boxes in their promoter region | (Zhou et al. 2008) |
| GmWRKY111 | Overexpression in soybean hairy roots enhances salt tolerance | (Xu et al. 2014) | |
| C2H2-type zinc finger protein | |||
| GmZAT4 | Overexpression in Arabidopsis enhances salt tolerance | GmZAT4 regulates the expressions of ABA-responsive marker genes including RD29A, RD29B, RAB, and ABI | (Sun et al. 2019b) |